Annual Cycle and Diversity of Species and Infraspecific Taxa of Ceratium (Dinophyceae) in the Ligurian Sea, Northwest Mediterranean1
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J. Phycol. 43, 1149–1163 (2007) Ó 2007 Phycological Society of America DOI: 10.1111/j.1529-8817.2007.00417.x ANNUAL CYCLE AND DIVERSITY OF SPECIES AND INFRASPECIFIC TAXA OF CERATIUM (DINOPHYCEAE) IN THE LIGURIAN SEA, NORTHWEST MEDITERRANEAN1 Alina Tunin-Ley, Jean-Philippe Labat, Ste´phane Gasparini, Laure Mousseau, and Rodolphe Leme´e2 Laboratoire d’Oce´anographie de Villefranche, Universite´ Pierre et Marie Curie-Paris 6, 06230 Villefranche-sur-Mer, France CNRS, Marine Microbial Ecology Group, Laboratoire d’Oce´anographie de Villefranche, 06230 Villefranche-sur-Mer, France We examined the well-documented and species- on. The first monograph was published in the rich dinoflagellate genus Ceratium Schrank in the beginning of the 20th century (Jørgensen 1911) fol- northwest Mediterranean Sea as a possible model lowed by many other taxonomic studies. Ceratium for marine phytoplankton diversity and as a bio- ranges from polar to tropical waters, in open sea as logical indicator of global climate change. First, we well as in neritic areas (Sournia 1967, Dodge and investigated the influence of counting effort; we Marshall 1994). Since it often represents a signifi- then documented temporal changes in Ceratium spe- cant part of the microphytoplankton in terms of cific and infraspecific taxa over 2 years (2002 and abundance and diversity, especially within the the- 2003) in the Villefranche Bay based on a monthly cate dinoflagellates, it plays a significant role in bio- net sampling. Finally, we tried to identify factors geochemical cycles. Furthermore, some species of associated with shifts in biodiversity. The calculation Ceratium are known to form red-tide blooms (Bocks- of taxonomic diversity, regularity, and richness were tahler and Coats 1993). The genus is very species highly dependent on counting effort. We deter- rich, with many species described from tropical and mined that a minimal sample volume of 70 L was subtropical areas (Dodge and Marshall 1994). A needed to obtain a good estimation of species rich- considerable amount of ecophysiological data exists ness. The annual cycle was characterized by a sea- as some common Ceratium species have been used sonal trend of high winter species richness followed in experimental and in situ studies ranging from by low spring biodiversity. Infraspecific variability investigations of bioluminescence (Sullivan and not only appeared to depend on water temperature Swift 1995) to cell division and growth rates but also seemed to be influenced by bottom-up con- (Elbra¨chter 1973, Weiler and Eppley 1979, Weiler trol and was strongly affected by top-down control. 1980), cellular functioning (Sato et al. 2004), tro- Thus, the occurrence of high concentrations of phic relationships (Smalley et al. 1999, 2003, Skovg- salps (Thalia democratica) and copepods larger than aard et al. 2000), and taxonomy (Sournia 1967). 2mm(Calanus helgolandicus) coincided with a dras- The genus has been also used as a biological indica- tic decrease of Ceratium abundance and diversity tor of water masses in the North Atlantic Ocean during spring 2003. Ceratium is sensitive to both abi- (Dodge and Marshall 1994, Raine et al. 2002), in otic and biotic factors and could prove to be a good the Pacific Ocean (Dodge 1993, Sanchez et al. candidate as a biological indicator of global change. 2000), in the Mediterranean Sea (Dowidar 1973), and in the Arctic Ocean (Okolodkov 1996). How- Key index words: annual cycle; Ceratium; dinofla- ever, like many planktonic groups, little is known gellates; diversity; infraspecific variability; Medi- about factors influencing the biodiversity of this terranean Sea; predation pressure genus, although it is characterized by a large num- Abbreviations: BIOSOPE, Biogeochemistry and ber of species and infraspecific taxa. While some Optics South Pacific Experiment; CA, correspon- taxonomic and biogeographical studies have tried dence analysis; CNRS, Centre National de la to assess the species richness of Ceratium in particu- Recherche Scientifique; CPR, continuous plank- lar areas (Sournia 1967, Dodge 1993, Semina and ton recorder; CTD, conductivity-temperature- Levashova 1993, Dodge and Marshall 1994), there is density; DOM, dissolved organic matter very little information on temporal patterns and the dynamics of biodiversity at annual and interannual timescales for Ceratium, particularly in terms of In the Mediterranean Sea, the genus of armored infraspecific variability. dinoflagellates, Ceratium, a component of the micro- In this study, we first focused on the validation of phytoplankton, was described and studied very early an adequate methodological approach for studying the genus Ceratium in terms of occurrence and biodiversity; more particularly, we tried to deter- 1Received 23 October 2006. Accepted 14 May 2007. mine the minimal volume of water to analyze to 2Author for correspondence: e-mail [email protected]. obtain reliable biodiversity parameters. Second, we 1149 1150 ALINA TUNIN-LEY ET AL. described the annual variations of specific and infra- Identification and counting were completed to the infraspe- specific composition through 2 years of monthly cific level, using standard taxonomic studies (Gourret 1883, sampling in the Villefranche Bay. Third, we investi- Jørgensen 1911, 1920, Tre´gouboff and Rose 1957a,b, Halim 1960, Dodge 1982, Steidinger and Tangen 1997) and the gated the relationships between abiotic and biotic nomenclature established by Sournia (1967) as a reference. factors on population dynamics in Ceratium. The taxonomic authorities are presented in Table 1. All the infraspecific taxa and species of the genus Ceratium that are MATERIALS AND METHODS cited in the present study are illustrated in the work of Sournia (1967), and, if not, references for corresponding descriptions Study site and sampling. Sampling was conducted at Point B are given in Sournia (1967). For standardization, the same in the Villefranche Bay (Fig. 1), a long-term monitoring site. person counted all the samples. The station is situated in the mouth of the bay (43°41¢10¢¢ N, The morphological variability in the genus Ceratium often 7°19¢00¢¢ E) and is not sheltered from the wind (Nival and exacerbates problems of nomenclature for infraspecific taxa. Corre 1976). The depth of sampling site is 86 m. At Point B, Thereby, an unofficial nomenclature was proposed, defined as physical, chemical, and biological parameters of the water a ‘‘para-taxonomic designation […] on the margin of the column (temperature, chl a, salinity, and main nutrient Linnaean nomenclature’’ by Sournia (1966, p. 1983). The concentrations) were determined weekly using a Seabird monograph of Sournia (1967) includes the description of SBE25 CTD (conductivity–temperature–density; Sea-Bird Elec- varieties, and transitional forms between these varieties, tronics Inc., Bellevue, Washington, USA) for vertical profiles which he characterized as showing a thermal preference and Niskin bottle water samples at six depths (75, 50, 30, 20, 10, (psychrophilic or thermophilic), and forms whose occurrence and 0 m). For statistical analysis, we used minimal, maximal, appears to be independent of the water temperature. For and integrated T (temperature), with integrated T as follows: Z example, the species Ceratium candelabrum is divided into two 1 varieties, C. candelabrum var. candelabrum (type species) and T ¼ Tdz z C. candelabrum var. depressum, and three intermediate forms, C. candelabrum ‘‘candelabrum-depressum,’’ C. candelabrum ‘‘cande- where z is the vertical axis. labrum > depressum’’ (nearer to the variety candelabrum), and A monthly phytoplankton sampling was conducted from C. candelabrum ‘‘depressum > candelabrum’’ (nearer to the variety December 2001 to December 2003. A 0–80 m sampling in depressum). In our study, the infraspecific taxa were distin- double oblique angle was performed with a custom-made guished using this nomenclature, except for C. fusus because conical phytoplankton net (53 lm mesh size, 54 cm diameter the descriptions of its infraspecific taxa vary considerably in the and 280 cm length). The volume filtered by the net was literature (Gourret 1883, Jørgensen 1911, 1920, Tre´gouboff measured with a TSK mechanical flowmeter (Tsurumi-Seiki Co. and Rose 1957a,b, Sournia 1967). Ltd., Yokohama, Japan). The volume sampled depended on The abundance of the rest of microphytoplankton, mainly the intensity of current. The sample was split once or twice diatoms, naked dinoflagellates, and silicoflagellates, was using a Motoda splitter (Motoda 1959), and the aliquot was estimated by integrating data based on Niskin water samples then fixed with acid Lugol’s solution (Throndsen 1978) to a at the six depths monitored at Point B between 0 and 80 m. 2% final concentration. The sample was finally divided into The six samples were mixed in relative proportions to the three replicates to reduce the bias resulting from manual corresponding water column to obtain a single sample per homogenization before counting. Although most phytoplank- date integrating the water column between 0 and 80 m, ton studies based on a net sampling are limited to a qualitative which allows the comparison with net samples. The samples approach, a quantitative analysis is possible when the filtered were concentrated by using the U¨ termohl method (Hasle water volume and the collected water volume are known. Thus, 1978) with an inverted microscope (Axiovert 35; Carl we could estimate the in situ abundance of each taxon in each Zeiss AG. Oberkochen, Germany) at ·200 and ·400 magni- sample.